In human and nonhuman primates social behavior varies between individuals, yet the genetic and evolutionary basis of this heterogeneity remains poorly understood. Our goal is to determine genetic contributions to variation in social behavior in rhesus macaques living in a naturalistic setting on Cayo Santiago Island, Puerto Rico. Initially, we focused on two questions. First, is sociality heritable and, if so, is this variation associated with genes previously linked to behavioral phenotypes in humans and captive primates? We used quantitative genetics to estimate the heritability of social network position. We then explored the association between sociality and two repeat polymorphisms in the serotonergic pathway: the gene encoding tryptophan hydroxylase (TPH2) and the 5HTTLPR polymorphism within the serotonin transporter gene (SLC6A4). Behavioral and genetic data were collected from 87 adult rhesus macaques in one group. Pedigrees were constructed using 29 microsatellite markers and length-polymorphisms assessed using PCRs. Using four social network measures, we found individuals’ positions within the aggression and affiliation (i.e. grooming and spatial proximity) networks demonstrated significant additive genetic variation and are thus heritable. This variation may be partly explained by serotonergic polymorphisms. Rhesus macaques with high-functioning TPH2 and 5HTTLPR alleles had significantly higher grooming network scores than individuals with low-functioning alleles. As the first large-scale study to examine behavior-genetic associations in a free-ranging primate, our results support the assumption that sociality has been shaped by selection acting on heritable variation and point to a potentially fundamental role of the serotonin pathway in the evolution of sociality in primates.

This work is supported by the National Institutes of Health (grant no. 1R01-MH-089484-01) and by the Duke Center for Interdisciplinary Decision Sciences.